Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse

Abstract

Maternal behaviour has profound, long-lasting implications for the health and well-being of developing offspring. In the monogamous California mouse (Peromyscus californicus), care by both parents is critical for offspring survival. We tested the hypothesis that similar to maternal care in rodents, paternal huddling and grooming (HG) behaviour can be transmitted to future generations via behavioural mechanisms. In California mice, testosterone maintains paternal HG behaviour. In the present study, we randomly assigned a group of male California mice to castration or sham-operated conditions and allowed them to raise their offspring normally. Adult sons of these males were paired with a female, and they were observed interacting with their own offspring. We found that like their fathers, the sons of castrated males huddled and groomed their young at lower levels than the sons of sham-operated fathers. The sons of castrates also retrieved pups more frequently. When both parents were present, the sons of castrates also showed a trend towards engaging in less exploratory behaviour. These data support the hypothesis that paternal behaviour, like maternal behaviour, can be transferred to future generations via epigenetic mechanisms and suggest that in a biparental species both parents contribute to offspring behavioural development.

Paternal Care in Biparental Rodents: Intra- and Inter-individual Variation

“…In the same species, castration reduces and testosterone replacement increases paternal behavior as well as AVP expression in the MeA, BNST, LS and LHN (Wang and De Vries 1993;De Vries and Miller 1999). In California mice, low levels of paternal behavior in adult sons of castrated males are associated with low expression of AVP in the dorsal BNST (Frazier et al 2006;Gleason and Marler 2013).…”

“…In another crossfostering study, male meadow voles raised by prairie vole foster parents received higher levels of parental care during pre-weaning development and subsequently performed more paternal behavior toward their own offspring, compared to male meadow voles raised by conspecific foster parents (McGuire 1988). Gleason and Marler (2013) characterized paternal behavior performed by castrated and sham-castrated California mouse fathers and, subsequently, by their sons. When tested in their home cage with one of their pups, castrated fathers took significantly longer than intact fathers to approach and begin caring for their pups, and spent significantly less time huddling and grooming their pups.…”

Early-Life Experience, Epigenetics, and the Developing Brain

“…These behavioral impairments are associated with paternal deprivation-induced neurobiological changes, including sex-specific effects on dopamine receptor gene expression in the nucleus accumbens , reductions in oxytocin receptor and ER alpha (ERa) levels (Cao et al, 2014), altered development of neuroendocrine pathways involved in the response to stress (Seidel et al, 2011), and reduced neuronal complexity (Braun et al, 2013;Pinkernelle et al, 2009). In the biparental California mouse, paternal behavior has been shown to alter the development of neural systems involved in aggression, with implications for variation in paternal behavior in male offspring (Frazier et al, 2006;Gleason and Marler, 2013). Manipulations of the quantity of paternal care in California mice, through use of a high foraging demand, leads to impairment in offspring learning and memory, increased indices of anxiety-like behavior, and altered synaptic development (Bredy et al, 2007).…”

Paternal care in a fish: epigenetics and fitness enhancing effects on offspring anxiety

“…Mother rats showing low levels of licking and grooming have offspring with increased DNA methylation of particular genes such as the glucocorticoid receptor (GR) in the hippocampus, resulting in decreased GR expression and an increased stress response [2,4]. Despite evidence in mammals that maternal care can influence offspring behaviour via epigenetic alterations to the genome, it remains unclear whether paternal care has similar effects ( [12], but see [13]). …”